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Platyrrhine Phylogenetics with a Focus on Callitrichine Life History Adaptations Natalie Mae Jameson Wayne State University

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Platyrrhine Phylogenetics with a Focus on Callitrichine Life History Adaptations Natalie Mae Jameson Wayne State University Wayne State University Wayne State University Dissertations 1-1-2013 Platyrrhine Phylogenetics With A Focus On Callitrichine Life History Adaptations Natalie Mae Jameson Wayne State University, Follow this and additional works at: http://digitalcommons.wayne.edu/oa_dissertations Part of the Evolution Commons Recommended Citation Jameson, Natalie Mae, "Platyrrhine Phylogenetics With A Focus On Callitrichine Life History Adaptations" (2013). Wayne State University Dissertations. Paper 844. This Open Access Dissertation is brought to you for free and open access by DigitalCommons@WayneState. It has been accepted for inclusion in Wayne State University Dissertations by an authorized administrator of DigitalCommons@WayneState. PLATYRRHINE PHYLOGENTICS WITH A FOCUS ON CALLITRICHINE LIFE HISTORY ADAPTATIONS by NATALIE MAE JAMESON DISSERTATION Submitted to the Graduate School of Wayne State University, Detroit, Michigan in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY 2013 MAJOR: MOLECULAR BIOLOGY & GENETICS Approved by: __________________________________ Advisor Date © COPYRIGHT BY NATALIE MAE JAMESON 2013 All Rights Reserved DEDICATION To my soon-to-be husband Chris, who knew that most bad days could be remedied with a crab leg dinner. ii ACKNOWLEDGMENTS Firstly, I thank my adviser, Derek Wildman. The education I received and the opportunities were afforded to me over my time in the Wildman lab will no doubt drive me to success throughout my career. Secondly, thank you to my committee members, Dr. Heng, Dr. Uddin, and Dr. Yi. It is because of their continual input and support that this research has been shaped into a body of work I am deeply proud of. Thank you to the staff of the Center for Molecular Medicine and Genetics, without whose help and backing I would have been lost. I will be forever grateful to the Wildman lab members, both past and present. Their valuable advice and unwavering friendships have been vital in carrying me through this process. I honor the memory of Dr. Morris Goodman, a brilliant scientist and wonderful man. I will always feel privileged for the time that I was able to learn from him. Finally I’d like to thank my family and friends. You know who you are and you know all you’ve done. Thank you, I love you all. iii TABLE OF CONTENTS Dedication ……………………………………………………………………………………… ii Acknowledgments …………………………………………………………………………….. iii List of Tables ………………………………………………………………………………….. v List of Figures ………………………………………………………………………………… vii Chapter 1: Introduction …………………………………………………………………..…… 1 Chapter 2: Genomic data reject the hypothesis of a prosimian primate clade (Published September 2011) ………………………………………………….. 11 Chapter 3: Development and annotation of shotgun sequence libraries from New World monkeys (Published September 2012) ……………………………….. 41 Chapter 4: The tempo and mode of New World monkey evolution and biogeography in the context of phylogenomic analysis (In review at Molecular Phylogenetics and Evolution) ………………………………………………….. 53 Chapter 5: Genetic underpinnings of litter size reduction in Goeldi’s monkey (Callimico goeldii) …………………………………………………………………….…… 95 Chapter 6: Conclusions ………………………………………………………………….… 128 Appendix A: Chapter 2 Supplemental Material …………………………………….…… 132 Appendix B: Chapter 3 Supplemental Material ……………………………………….… 135 Appendix C: Chapter 4 Supplemental Material …………………………………….…… 136 Appendix D: Chapter 5 Supplemental Material ……………………………………….… 140 References ………………………………………………………………………………….. 144 Abstract ………………………………………………………………………………….….. 188 Autobiographical Statement ………………………………………………………….…… 190 iv LIST OF TABLES Table 2.1: Presence of selected character states that vary among the three major primate clades …………………….…………………………....……………….. 17 Table 2.2: Mammalian taxa used to infer the phylogeny ………………….…………….. 21 Table 2.3: Divergence date estimates and 95% credibility intervals ……...………...…. 31 Table 3.1: Shotgun library composition ……………………………...……………………. 49 Table 4.1: Taxon sampling ..…………..……………………………….………………...…. 58 Table 4.2: Divergence dates at nodes ….…………………………….………………...…. 71 Table 4.3: Rate variation …….…………………………………………………………...…. 72 Table 5.1: Shared derived traits in Cebidae ……...………….………………………...…. 96 Table 5.2: New World monkey tissue samples ……………..………………………...….. 99 Table 5.3: Genes involved in reproduction and ovulation ……...…………………...…. 103 Table 5.4: Microsatellite genotyping results …………………….…………………...….. 109 Table 5.5: RNAseq summary statistics ……………………………….……………...….. 115 Table 5.6: Genes undergoing adaptive evolution within callitrichines ……………...….117 Table 5.7: Codon sites undergoing accelerated evolution ….……………………...….. 119 Table S1: Full list of taxa used in divergence dating analyses ...……………………… 132 Table S2: Nucleotide composition in the 47 transcript and the 1,078 transcript datasets ….……………………………………………………………………… 133 Table S3: Divergence date estimates and 95% credibility intervals for all taxa using mcmctree .….……………………………………………………….…………… 133 Table S4: Divergence date estimates and 95% credibility intervals for 17 mammalian taxa in BEAST using the 47 transcript dataset ..….…..………….………… 134 Table S5: Repetitive elements identified within sequencing reads …………..…….… 135 v Table S6: Primers for 64 non-genic markers ………………………….…………….….. 136 Table S7: Division of partitions based on GC content ……………..……………….….. 137 Table S8: Annotation of non-genic markers …………………………...…………….….. 138 Table S9: Species coverage for each gene analyzed in PAML ……..…………….….. 140 vi LIST OF FIGURES Figure 2.1: Four hypotheses for the phylogenetic relationships among the three major primate clades ..……………………………………………….……………….. 14 Figure 2.2: Anthropoid phylogenetic tree ..…………………………...…………………… 29 Figure 2.3: Topology test supporting the grouping of Tarsius with Anthropoidea ..…... 30 Figure 2.4: Divergence dates estimates in Euarchontoglires ...…....…………………… 31 Figure 3.1: Representative New World monkey species ..………………………….…... 44 Figure 3.2: Workflow showing the steps involved in the shotgun library construction, sequencing, and annotation ..…................................................................. 47 Figure 4.1: Geographic ranges and distributions of New World monkeys ..….............. 64 Figure 4.2: Phylogeny of extant NWM species ..…....................................................... 67 Figure 4.3: Divergence date analysis ………................................................................. 70 Figure 4.4: Ancestral area reconstruction …….............................................................. 73 Figure 4.5: Depiction of clade distribution throughout South America ……................... 75 Figure 4.6: Phylogenetic resolution within Aotus .......................................................... 81 Figure 4.7: Hypothesized migratory routes to the Neotropics ………..…………………. 83 Figure 5.1: Evolution of offspring number variation …………………………….…….….. 97 Figure 5.2: Sliding window sequence quality check ..……………………...……….….. 105 Figure 5.3: Branch test models of adaptive evolution ……………………...……….….. 107 Figure 5.4: Branch-sites test model of adaptive evolution …………………...…….….. 108 Figure 5.5: SRY amplification ……………………………………………………...….….. 114 Figure 5.6: Genes undergoing adaptive evolution on callitrichine lineages ……….… 117 Figure 5.7: Genes with sites undergoing adaptive evolution on callitrichine lineages .118 vii Figure S1: Optimal models of sequence evolution selected for each transcript in both datasets .……………………………………………………...……….…….…. 132 Figure S2: Distribution of sequencing reads among human chromosomes based on BLAST search results ……….……………………………...…...………….… 135 Figure S3: Pedigree of Callimico goeldii individuals tested for chimerism …….…….. 143 viii 1 CHAPTER 1 Introduction Understanding reproductive strategies is a central aspect in studies of species evolution (Kappeler et al., 2003). The unique assemblage of a species’ life history traits defines its reproductive strategy. Life history traits having a major influence on reproductive strategy are those such as, number versus quality of offspring, current versus future reproduction, age versus size at maturity, and fecundity versus lifespan. Drastic changes in traits such as these occur on a long evolutionary time scale (i.e. between Orders), while smaller adjustments to these traits can occur in shorter time (i.e. within an Order) (Promislow and Harvey, 1990). However there are exceptions, such as litter size within the Order Primates. Within Primates, litter size varies from 1 to 4 offspring per pregnancy; with the majority of species producing singleton offspring (Leutenegger, 1979). Interestingly, species within Cebidae (squirrel monkey, capuchin monkey, owl monkey, marmoset, tamarin, and Goeldi’s monkey) produce litters that span the full spectrum of one to four offspring (Ross, 1991). The variation in litter size seen among the relatively closely related Cebidae species suggests an alteration of reproductive strategies within the past 10 million years (Opazo et al., 2006; Perelman et al., 2011; Jameson et al., In Review, See chapter 4). The aim of my research is to integrate phenotypic and genotypic character evolution in order to determine the molecular underpinnings of reproductive strategies in New World monkeys. I have employed the use of comparative genomics, tracing the 2 evolution of genes and phenotypes on the background of a well resolved phylogeny to determine conserved and derived character states, which has been shown to be a valuable
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